- Email: [email protected]
Secondary cell wall patterning during xylem differentiation
Available online at www.sciencedirect.com
Secondary cell wall patterning during xylem differentiation Yoshihisa Oda and Hiroo Fukuda Xylem cell differentiation involves temporal and spatial regulation of secondary cell wall deposition. The cortical microtubules are known to regulate the spatial pattern of the secondary cell wall by orientating cellulose deposition. However, it is largely unknown how the microtubule arrangement is regulated during secondary wall formation. Recent findings of novel plant microtubule-associated proteins in developing xylem vessels shed new light on the regulation mechanism of the microtubule arrangement leading to secondary wall patterning. In addition, in vitro culture systems allow the dynamics of microtubules and microtubuleassociated proteins during secondary cell wall formation to be followed. Therefore, this review focuses on novel aspects of microtubule dynamics leading to secondary cell wall patterning with a focus on microtubule-associated proteins. Address Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan Corresponding authors: Oda, Yoshihisa ([email protected]) and Fukuda, Hiroo ([email protected])
Current Opinion in Plant Biology 2012, 15:38–44 This review comes from a themed issue on Growth and Development Edited by Xuemei Chen and Thomas Laux Available online 9th November 2011 1369-5266/$ – see front matter Published by Elsevier Ltd. DOI 10.1016/j.pbi.2011.10.005
SND1/NST3 and NST1 were also identified as master regulators for xylem fiber differentiation [5–7]. These transcription factors form a subgroup in the NAC family [8,9]. Ectopic expressions of these genes induce ectopic deposition of secondary walls in accordance with their cell fates, for example, spiral and annular secondary walls by VND7, pitted secondary walls by VND6, and flat secondary walls by SND1 [10,11,12,13]. Further analyses demonstrate that NAC-type master transcription factors regulate the secondary wall synthesis as their downstream events [11,13]. Therefore, xylem cell differentiation involves molecular mechanisms underlying dynamic formation of cell wall structures. Additionally the use of these master genes in in vitro culture resulted in establishment of novel xylem cell differentiation systems [10,11]. It is well known that the secondary wall pattern is determined by cortical microtubules (MTs) that direct the movement of cellulose synthase complexes on the plasma membrane [14]. However, the machinery by which cortical MTs are arranged to form specific secondary wall patterns is largely unknown. Recently, some important plant MT-associated proteins (MAPs) were identified in relation to the secondary wall patterning. For example, AtMAP70 family proteins are involved in the formation of the secondary wall boundary [15]. MIDD1/RIP3 promotes MT depolymerization in future secondary wall pit areas, resulting in a secondary wall depletion domain [10]. These findings shed new insight into the MT organization mechanism regulating secondary wall patterning. Therefore, in this review we summarize recent progress of studies on secondary wall patterning with a focus on MAPs.
Introduction
MT organization in xylem vessel cells
Tracheary elements are characterized by their elaborate morphology and are the major conductive component of xylem, which functions in the transport of water and nutrients from the root to the whole plant body. Tracheary elements are dead cells surrounded by rigid patterned cellulosic secondary cell walls beneath the primary walls [1]. In tracheary elements, secondary walls are deposited in various patterns, such as annular and spiral in protoxylem, and reticulate and pitted patterns in metaxylem (Figure 1) [2]. Thus, secondary wall pattern is an important character of different xylem cells.
Most cortical MTs run beneath the secondary wall thickening whereas few cortical MTs lie beneath the region between the secondary walls. Disruption of MTs by drug treatments disorganizes secondary wall patterns, suggesting that cortical MTs regulate secondary wall patterning [16,17]. In Arabidopsis root vessels, cortical MTs are necessary for targeting cellulose synthase complexes to the specific sites through vesicle transport along actin cables [18–20]. These cortical MTs probably function in targeting the vesicles that contain cellulose synthase complexes and in controlling the trajectory of cellulose synthase complexes as observed in hypocotyl epidermis [14,21,22].
Xylem cell fates are controlled by transcriptional master genes [3]. Two NAM/ATAF/CUC (NAC) transcription factors, VND6 and VND7, direct metaxylem and protoxylem vessel differentiation, respectively [4]. Current Opinion in Plant Biology 2012, 15:38–44
Studies using the in vitro culture of isolated Zinnia mesophyll cells [23] visualized dynamic changes of the www.sciencedirect.com
Secondary cell wall patterning during xylem differentiation Oda and Fukuda 39
Figure 1
secondary wall formation and to know their function. In this context, some important secondary wall-related MAPs have been discovered. We describe below such MAPs after categorizing them into four classes according to their function.
MAPs involved in cortical MT assembly Katanin is an MT-severing MAP that is involved in cortical MT organization in both non-xylem and xylem cells. The Arabidopsis genome encodes a katanin gene, AtKTN1, whose mutation causes global disorganization of the cortical MT array and cellulose microfibril arrays in secondary and primary cell walls resulting in cell deformation and short organs [27,28]. In Arabidopsis hypocotyl epidermis cells, AtKTN1 is required to release the nucleated MTs from gamma tubulin complexes that are recruited beside existing cortical MTs [29]. Although it is not clear whether katanin functions in xylem cells similarly to those in hypocotyl epidermis cells, MT nucleation and severing should be an important process to organize the cortical MTs into distinct patterns of secondary wall deposition.
Current Opinion in Plant Biology
A collection of secondary wall patterns of xylem vessels in Arabidopsis plants. From left: spiral, reticulate, scalariform, and two pitted patterns. Scale bar represents 10 mm.
cortical organization of MTs during secondary wall formation in developing tracheary elements and confirmed that secondary wall patterns reflect the preceding localization of cortical MTs [24]. Recently, two Arabidopsis xylogenic culture systems were established: a culture in which boron and/or plant hormones are used as inducers of tracheary element differentiation [4,15,25] and a VND6-harboring culture in which estrogen induces VND6 and then metaxylem vessel differentiation [10]. These cultures allowed to introduce various cytoskeleton-related genes and follow the dynamics of their gene products during secondary wall deposition. By using cultures expressing GFP-tubulin, it was revealed that cortical MTs are gradually bundled and then followed by secondary wall deposition [25,26]. In differentiating cultured metaxylem vessel cells, rescue events of cortical MTs are inhibited in the future pit area, which causes the local disassembly of MTs to form an MT-free area [10]. These findings suggest that MT organization is regulated, at least in some part, in a secondary wall-specific manner. Therefore, it is important to find MAPs involved in www.sciencedirect.com
ZeMAP65-1 and AtMAP65-8, members of the MAP65 protein family, are preferentially expressed in xylogenic Zinnia mesophyll cells and Arabidopsis suspension cells, respectively [4,30]. An antibody against the conserved peptide of MAP65 proteins detects bundled cortical MTs in differentiating xylem cells [30]. Ectopic expression of ZeMAP65-1 in Arabidopsis cultured cells induces massive bundling of cortical MTs [30]. Therefore, these MAP65 members must be responsible for the bundling of the cortical MTs in xylem vessels. Because carrot MAP65 and AtMAP65-1, other members of the MAP65 protein family that act in non-xylem cells, also induce MT bundles by cross-linking each other [31,32], in general, this family may function in the assembly of MTs.
MAPs involved in oriented cellulose deposition FRA1, which encodes a kinesin motor protein of the kinesin-4 family, is expressed strongly in xylem, meristems, and parenchyma [33,34]. The mutation in the FRA1 locus decreases the mechanical strength of interfascicular fibers due to disorganization of cellulose microfibril alignment in the secondary walls. However, fra1 mutants do not differ significantly from the wild type in secondary wall composition, secondary wall thickness, or cortical MT organization [33]. Overexpression of FRA1 in plants increases layers of secondary walls with a remarkable decrease in the thickness of each secondary wall layer in xylem cells [34]. Because the number of secondary wall layers is dependent on changes in the orientation of cellulose microfibrils, all of these data suggest that FRA1 may function in the oriented deposition of cellulose microfibrils probably by regulating the cellulose synthesis machinery or the transport of vesicles carrying the secondary wall materials [34]. Current Opinion in Plant Biology 2012, 15:38–44
40 Growth and Development
Another MAP involved in secondary wall deposition is Populus MAP20 (PttMAP20), which is a plant-specific small protein containing a conserved TPX2 domain. PttMAP20 is co-upregulated in all types of populous xylem cells [35] with the secondary wall-associated cellulose synthase genes. PttMAP20 directly binds MTs in vitro and decorates MTs in vivo. Overexpression of PttMAP20 results in twisted shoot organs and shorter roots as frequently observed in plants in which other MAPs are overexpressed. Although the exact function of PttMAP20 is still to be demonstrated, a cellulose synthesis inhibitor 2,6dichlorobenzonitrile (DCB) was found to bind to PttMAP20 [35]. Recently, DCB treatment was shown to inhibit the mobility of cellulose synthase complexes at the plasma membrane [36]. Because DCB does not inhibit MT binding of PttMAP20, PttMAP20 may promote the activity of the cellulose synthesis along cortical MTs [35].
MAPs defining the boundary of secondary walls MAP70-5 and MAP70-1 belong to the plant-specific 70 kDa MAP family [37,38]. MAP70-5 was found to be specifically expressed during xylem differentiation in comprehensive expression analysis for over 200 MAPs using newly established xylogenic Arabidopsis cell culture [15]. Although MAP70-1 is constitutively expressed in the cell culture, these two proteins interact with each other and function in secondary wall patterning [15]. Overexpression of MAP70-5 and/or MAP70-1 increases the population of xylem cells with spiral secondary walls. By contrast, the knockdown for MAP70-5 or MAP70-1 by RNA interference increases the population of xylem cells
with pitted secondary walls. Knockdown for MAP70-5 or MAP70-1 causes dissociation of secondary wall thickenings from the plasma membrane in all types of the tracheary element. Indeed, MAP70-1 and MAP70-5 proteins appear to localize at the subpopulation of cortical MTs along the edge of secondary wall thickenings. On the basis of these results, the authors suggest that MAP70 proteins define the boundary of secondary wall deposition on the plasma membrane. Considering that MAP70-5 was indicated to stabilize MTs [38] and that similar patterns of secondary walls were observed in taxol-treated cells [25], one might assume that MAP70-5 protein affects secondary wall patterns by stabilizing cortical MTs. The mechanism of the distinct localization of these proteins remains to be determined.
MAPs preventing secondary wall deposition Using the VND6-inducible metaxylem vessel differentiation culture, MIDD1 was identified as a MAP that regulates secondary wall patterns [10]. MIDD1 is upregulated rapidly by VND6 and VND7, which induce metaxylem and protoxylem vessel differentiation, respectively [10,11]. MIDD1 directly binds MTs in vitro [10]. However, in differentiating metaxylem vessel cells, MIDD1 decorates only the subpopulation of cortical MTs in the secondary wall pits (Figure 2a). MIDD1 is a plant-specific small protein composed of only two coiled-coil domains. Domain analysis revealed that the first coiled-coil domain binds MTs and the second coiledcoil domain recognizes the plasma membrane domain beneath the secondary wall pits. Knockdown of MIDD1
Figure 2
(a)
MT
MIDD1
0 sec
72
48
24
96
(b)
Secondary wall
Pri r mary wall ri Pla asma s sm membr m ane
ROP MT MT
MT
MT
?
MIDD1 AtKinesin-13A
? Current Opinion in Plant Biology
Dynamics and function of MIDD1. (a) Time-lapse observation of cortical MTs (RFP-TUB6) and MIDD1 (MIDD1-GFP) in the differentiating xylem cell. Yellow arrowheads indicate growing MTs that are specifically labeled with MIDD1. Red arrowheads indicate shrinking MTs. Scale bar represents 2 mm. (b) Schematic illustration of a possible model for MIDD1 function. In this model, MIDD1 is anchored to the plasma membrane in secondary wall pits by GTP-bound ROPs, recruits AtKinesin-13A, and binds cortical MTs in the secondary wall pits to promote disassembly of cortical MTs. Current Opinion in Plant Biology 2012, 15:38–44
www.sciencedirect.com
Secondary cell wall patterning during xylem differentiation Oda and Fukuda 41
with RNAi causes failure of local MT disassembly, which results in producing pit-free flat secondary walls. Conversely, overexpression of MIDD1 decreases the density of cortical MTs. These results strongly suggest that MIDD1 is a crucial factor for MT disassembly in secondary wall pits [10]. It was reported that MIDD1 interacts with AtKinesin13A, a member of the Kinesin-13 family [39]. Animal Kinesin-13 proteins depolymerize MTs in an ATP-dependent manner [40,41]. AtKinesin-13A lacks the conserved neck region that is necessary for interaction between the motor domain and MTs to exert MT depolymerization activity [42]. Therefore, AtKinesin-13A is
unlikely to have MT depolymerization activity [41]. Indeed, this protein does not exhibit MT colocalization but localized to the Golgi apparatus [43]. However, it is plausible that MIDD1 combines AtKinesin-13A to cortical MTs and allows it to work for MT depolymerization. MIDD1 is accumulated at the MT plus end during MT shrinkage [10]. Similarly, Drosophila KLP59C, a member of Kinesin-13, accumulates at the MT plus end during MT shrinkage [44]. Therefore, a member (or members) of the plant Kinesin-13 family might depolymerize MTs together with MIDD1. Further studies are required to test this possibility.
Figure 3
Production of plasma membrane domains ROPs?
Local MT disassembly Without MIDD1
MIDD1 Kinesin-13A?
MIDD1
MAP70
Control of secondary wall boundary? MAP70 Cortical MT organization Katanin MAP65?
Oriented deposition of cellulose microfibrils MAP20 ? FRA1
Current Opinion in Plant Biology
A schematic illustration for a template organization model for secondary wall patterning. First, plasma membrane domains are produced by ROPs as a robust template for secondary wall patterns. Second, MIDD1 is recruited to the plasma membrane domains to promote local disassembly of cortical MTs. MAP70 may organize cortical MTs to define the boundary for secondary wall deposition to shift the secondary wall pattern. Katanin and MAP65 organize the cortical MTs through severing and bundling beneath the future secondary wall thickening. Finally, FRA1 and MAP20 control the oriented deposition of the cellulose microfibrils along the cortical MTs. www.sciencedirect.com
Current Opinion in Plant Biology 2012, 15:38–44
42 Growth and Development
The pit-specific MT association of MIDD1 depends on its second coiled-coil domain, which is anchored to the plasma membrane in secondary wall pits [10]. MIDD1 is a member of the ICR/RIP family of proteins, which are shown to interact with plant-specific Rac/Rho small GTPases (ROPs) [45,46]. Recently, it was demonstrated that MIDD1 is a ROP effector that binds to the GTP-bound form of ROPs [39]. It is well known that ROPs are localized at specific plasma membrane domains and are involved in cell polarity [47]. Regarding cortical MTs, ROP6 recruits its effector RIC1, which locally induces ordered cortical MTs to form indentations of leaf epidermal cells [48,49]. Therefore, it is plausible that ROPs anchor MIDD1 at the discrete plasma membrane domains. Indeed, deletion of the Cterminal part of the second coiled-coil domain comprising the ROP binding motif was enough to abolish their anchorage at the plasma membrane [10]. In summary, MIDD1 is likely to act as a scaffold protein that bridges a ROP, a Kinesin-13 and cortical MTs (Figure 2b).
Template organization model Recent studies of secondary wall patterning have focused on cortical MTs, MAPs, and cellulose synthesis. However, identification and characterization of MIDD1 raises another possibility, namely that distinct plasma membrane domains also participate in the secondary wall patterning. Such plasma membrane domains may localize specific molecules that affect MT organization and secondary wall deposition, which thereby act as a robust template for secondary wall patterns. As described above, ROPs are good candidate molecules for producing plasma membrane domains as a template. Indeed, small GTPases are involved in producing plasma membrane domains in yeast budding [50], cell migration [51], and neural development [52]. One possibility is that such templates of ROPs might be established stochastically by Turing’s reaction diffusion model [53]. Once such a template is organized, MIDD1 is recruited to the plasma membrane domains by the ROPs and then depolymerizes the cortical MTs on the template. Subsequently, MAP70 may organize cortical MTs to define the boundary for secondary wall deposition to shift the secondary wall pattern. Considering the difference between the RNAi phenotypes for MIDD1 and MAP70s, MIDD1 and MAP70s may not function antagonistically but rather, function in different stages: MIDD1 promotes local depletion of cortical MTs while MAP70s modify the shape of the MT-depleted domains. Then, katanin and MAP65 organize the cortical MTs through severing and bundling beneath the future secondary wall thickening. Finally, FRA1 and MAP20 control the orientation of the cellulose microfibrils upon the cortical MTs (Figure 3).
wall patterns. Further analysis of ROPs as a templateproducing candidate would be promising to prove the template model. Nevertheless, our knowledge is still fragmentary. Further identification and characterization of other secondary wall-related proteins, including MAPs, are required to unveil fully the regulatory mechanism for secondary wall patterns. Because different xylem cell types have distinct secondary wall patterns, comparison of cytoskeleton-related genes downstream of master transcription factors inducing different xylem cell types may be useful for the identification of such proteins. Indeed, overexpression of VND6, VND7, and SND1 induces the expression of genes for different sets of kinesins (AT2G47500, AT5G06670, and AT4G38950 by VND7; AT2G47500, AT5G06670, At5G27950, and At5g54670 by VND6; At5G27950 and At5g54670 by SND1) in addition to MIDD1 and MAP65-8 [11,13]. Computational simulation analysis is also powerful in integrating insights into secondary wall patterning. Importantly, these insights into secondary wall patterning should contribute to advancing our understanding of secondary wall development and how plant cells produce distinct plasma membrane domains and then a variety of cell wall structures.
Acknowledgements This work was supported partly by Grants-in-Aid from the Ministry of Education, Science, Sports and Culture of Japan (19060009) to H.F., from the Japan Society for the Promotion of Science to H.F. (23227001) and Y.O. (22870005), and from Bio-oriented Technology Research Advancement Institution, Japan (BRAIN) to H.F.
References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest 1.
Fukuda H: Tracheary element differentiation. Plant Cell 1997, 9:1147-1156.
2.
Turner S, Gallois P, Brown D: Tracheary element differentiation. Annu Rev Plant Biol 2007, 58:407-433.
3.
Ohashi-Ito K, Fukuda H: Transcriptional regulation of vascular cell fates. Curr Opin Plant Biol 2010, 13:670-676.
4.
Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T: Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 2005, 19:1855-1860.
5.
Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M: NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 2007, 19:270-280.
6.
Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M: The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 2005, 17:2993-3006.
7.
Zhong R, Demura T, Ye ZH: SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 2006, 18:3158-3170.
8.
Demura T, Fukuda H: Transcriptional regulation in wood formation. Trends Plant Sci 2007, 12:64-70.
9.
Zhong R, Ye ZH: Regulation of cell wall biosynthesis. Curr Opin Plant Biol 2007, 10:564-572.
Conclusions and perspectives In this review, we described recent advances in studies on the regulatory mechanism of secondary wall patterning, with a special focus on MAPs, and provided a template model of MT organization leading to distinct secondary Current Opinion in Plant Biology 2012, 15:38–44
www.sciencedirect.com
Secondary cell wall patterning during xylem differentiation Oda and Fukuda 43
10. Oda Y, Iida Y, Kondo Y, Fukuda H: Wood cell-wall structure requires local 2D-microtubule disassembly by a novel plasma membrane-anchored protein. Curr Biol 2010, 20:1197-1202. The authors established a high efficiency in vitro differentiation system for metaxylem vessels by making transgenic Arabidopsis cultured cells with inducible VND6. The authors identified MIDD1/RIP3 as a MAP and found that MIDD1/RIP3 is required in local cortical MT disassembly for secondary wall pit formation. This study implies the potential involvement of ROP GTPase signaling in secondary wall patterning. 11. Ohashi-Ito K, Oda Y, Fukuda H: Arabidopsis VASCULAR RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation. Plant Cell 2010, 22:3461-3473. The authors compared target genes of VND6 and SND1 and revealed that they commonly regulate secondary wall-related genes whereas only VND6 upregulated PCD-related genes. They also clearly showed that VND6 induces the secondary wall deposition in metaxylem pattern while SND1 induces uniform secondary walls of xylem fibers. 12. Yamaguchi M, Goue N, Igarashi H, Ohtani M, Nakano Y, Mortimer JC, Nishikubo N, Kubo M, Katayama Y, Kakegawa K et al.: VASCULAR-RELATED NAC-DOMAIN6 and VASCULARRELATED NAC-DOMAIN7 effectively induce transdifferentiation into xylem vessel elements under control of an induction system. Plant Physiol 2010, 153:906-914. 13. Yamaguchi M, Mitsuda N, Ohtani M, Ohme-Takagi M, Kato K, Demura T: VASCULAR-RELATED NAC-DOMAIN7 directly regulates the expression of a broad range of genes for xylem vessel formation. Plant J 2011, 66:579-590. This study revealed direct and indirect targets of VND7 involved in a wide range of processes of xylem vessel differentiation and demonstrated that VND7 can induce secondary wall deposition in the protoxylem pattern while NST3 induces flat secondary walls of fibers. 14. Paredez AR, Somerville CR, Ehrhardt DW: Visualization of cellulose synthase demonstrates functional association with microtubules. Science 2006, 312:1491-1495. 15. Pesquet E, Korolev AV, Calder G, Lloyd CW: The microtubule associated protein AtMAP70-5 regulates secondary wall patterning in Arabidopsis wood cells. Curr Biol 2010, 20:744-749. The authors newly established an in vitro xylogenic cell culture from Arabidopsis roots and performed expression analysis for over 200 MAPs. They found that AtMAP70-5 is upregulated in their culture system and they analyzed the function of MAP70. This study demonstrated that the expression level of MAPs contributes to the secondary wall patterns. 16. Hepler PK: Morphogenesis of tracheary elements and guard cells. Cell Biol Monogr 1981, 8:327-347. 17. Gunning BES, Hardham AR: Microtubules. Annu Rev Plant Biol 1982, 33:651-698. 18. Gardiner JC, Taylor NG, Turner SR: Control of cellulose synthase complex localization in developing xylem. Plant Cell 2003, 15:1740-1748. 19. Wightman R, Turner SR: The roles of the cytoskeleton during cellulose deposition at the secondary cell wall. Plant J 2008, 54:794-805. 20. Wightman R, Marshall R, Turner SR: A cellulose synthasecontaining compartment moves rapidly beneath sites of secondary wall synthesis. Plant Cell Physiol 2009, 50:584-594. 21. Crowell EF, Bischoff V, Desprez T, Rolland A, Stierhof YD, Schumacher K, Gonneau M, Hofte H, Vernhettes S: Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 2009, 21:1141-1154. 22. Gutierrez R, Lindeboom JJ, Paredez AR, Emons AM, Ehrhardt DW: Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol 2009, 11:797-806. 23. Fukuda H, Komamine A: Establishment of an experimental system for the study of tracheary element differentiation from single cells isolated from the mesophyll of Zinnia elegans. Plant Physiol 1980, 65:57-60.
www.sciencedirect.com
24. Fukuda H, Kobayashi H: Dynamic organization of the cytoskeleton during tracheary-element differentiation. Dev Growth Differ 1989, 31:9-16. 25. Oda Y, Mimura T, Hasezawa S: Regulation of secondary cell wall development by cortical microtubules during tracheary element differentiation in Arabidopsis cell suspensions. Plant Physiol 2005, 137:1027-1036. 26. Oda Y, Hasezawa S: Cytoskeletal organization during xylem cell differentiation. J Plant Res 2006, 119:167-177. 27. Burk DH, Liu B, Zhong R, Morrison WH, Ye ZH: A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 2001, 13:807-827. 28. Burk DH, Ye ZH: Alteration of oriented deposition of cellulose microfibrils by mutation of a katanin-like microtubulesevering protein. Plant Cell 2002, 14:2145-2160. 29. Nakamura M, Ehrhardt DW, Hashimoto T: Microtubule and katanin-dependent dynamics of microtubule nucleation complexes in the acentrosomal Arabidopsis cortical array. Nat Cell Biol 2010, 12:1064-1070. This study revealed that katanin functions in severing the branched cortical MTs to release them from their mother MTs. 30. Mao G, Buschmann H, Doonan JH, Lloyd CW: The role of MAP651 in microtubule bundling during Zinnia tracheary element formation. J Cell Sci 2006, 119:753-758. 31. Chan J, Jensen CG, Jensen LC, Bush M, Lloyd CW: The 65-kDa carrot microtubule-associated protein forms regularly arranged filamentous cross-bridges between microtubules. Proc Natl Acad Sci USA 1999, 96:14931-14936. 32. Smertenko AP, Chang HY, Wagner V, Kaloriti D, Fenyk S, Sonobe S, Lloyd C, Hauser MT, Hussey PJ: The Arabidopsis microtubule-associated protein AtMAP65-1: molecular analysis of its microtubule bundling activity. Plant Cell 2004, 16:2035-2047. 33. Zhong R, Burk DH, Morrison WH 3rd, Ye ZH: A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 2002, 14:31013117. 34. Zhou J, Qiu J, Ye ZH: Alteration in secondary wall deposition by overexpression of the fragile fiber1 kinesin-like protein in Arabidopsis. J Integr Plant Biol 2007, 49:1235-1243. 35. Rajangam AS, Kumar M, Aspeborg H, Guerriero G, Arvestad L, Pansri P, Brown CJ, Hober S, Blomqvist K, Divne C et al.: MAP20, a microtubule-associated protein in the secondary cell walls of hybrid aspen, is a target of the cellulose synthesis inhibitor 2,6-dichlorobenzonitrile. Plant Physiol 2008, 148:1283-1294. 36. DeBolt S, Gutierrez R, Ehrhardt DW, Somerville C: Nonmotile cellulose synthase subunits repeatedly accumulate within localized regions at the plasma membrane in Arabidopsis hypocotyl cells following 2,6-dichlorobenzonitrile treatment. Plant Physiol 2007, 145:334-338. 37. Korolev AV, Chan J, Naldrett MJ, Doonan JH, Lloyd CW: Identification of a novel family of 70 kDa microtubuleassociated proteins in Arabidopsis cells. Plant J 2005, 42:547555. 38. Korolev AV, Buschmann H, Doonan JH, Lloyd CW: AtMAP70-5, a divergent member of the MAP70 family of microtubuleassociated proteins, is required for anisotropic cell growth in Arabidopsis. J Cell Sci 2007, 120:2241-2247. 39. Mucha E, Hoefle C, Hu¨ckelhoven R, Berken A: RIP3 and AtKinesin-13A: a novel interaction linking Rho proteins of plants to microtubules. Eur J Cell Biol 2010, 89:906-916. This paper demonstrated that MIDD1/RIP3 is the effector of ROP GTPases and interacts with AtKinesin-13A. 40. Desai A, Verma S, Mitchison TJ, Walczak CE: Kin I kinesins are microtubule-destabilizing enzymes. Cell 1999, 96:69-78. 41. Moores CA, Milligan RA: Lucky 13-microtubule depolymerisation by kinesin-13 motors. J Cell Sci 2006, 119:3905-3913.
Current Opinion in Plant Biology 2012, 15:38–44
44 Growth and Development
42. Ovechkina Y, Wagenbach M, Wordeman L: K-loop insertion restores microtubule depolymerizing activity of a ‘‘neckless’’ MCAK mutant. J Cell Biol 2002, 159:557-562. 43. Lu L, Lee YR, Pan R, Maloof JN, Liu B: An internal motor kinesin is associated with the Golgi apparatus and plays a role in trichome morphogenesis in Arabidopsis. Mol Biol Cell 2005, 16:811-823. 44. Mennella V, Rogers GC, Rogers SL, Buster DW, Vale RD, Sharp DJ: Functionally distinct kinesin-13 family members cooperate to regulate microtubule dynamics during interphase. Nat Cell Biol 2005, 7:235-245. 45. Lavy M, Bloch D, Hazak O, Gutman I, Poraty L, Sorek N, Sternberg H, Yalovsky S: A novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr Biol 2007, 17:947-952.
48. Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z: Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 2005, 120:687-700. 49. Fu Y, Xu T, Zhu L, Wen M, Yang Z: A ROP GTPase signaling pathway controls cortical microtubule ordering and cell expansion in Arabidopsis. Curr Biol 2009, 19:1827-1832. The paper demonstrated that local ROP signaling regulates cortical MTs at subcellular level to induce polarized cell growth. 50. Kozubowski L, Saito K, Johnson JM, Howell AS, Zyla TR, Lew DJ: Symmetry-breaking polarization driven by a Cdc42p GEF-PAK complex. Curr Biol 2008, 18:1719-1726. 51. Fivaz M, Bandara S, Inoue T, Meyer T: Robust neuronal symmetry breaking by Ras-triggered local positive feedback. Curr Biol 2008, 18:44-50.
46. Li S, Gu Y, Yan A, Lord E, Yang ZB: RIP1 (ROP Interactive Partner 1)/ICR1 marks pollen germination sites and may act in the ROP1 pathway in the control of polarized pollen growth. Mol Plant 2008, 1:1021-1035.
52. Wong K, Pertz O, Hahn K, Bourne H: Neutrophil polarization: spatiotemporal dynamics of RhoA activity support a selforganizing mechanism. Proc Natl Acad Sci USA 2006, 103:3639-3644.
47. Yang Z: Cell polarity signaling in Arabidopsis. Annu Rev Cell Dev Biol 2008, 24:551-575.
53. Turing A: The chemical basis of morphogenesis. Philos Trans R Soc Lond B Biol Sci 1952, 237:37-72.
Current Opinion in Plant Biology 2012, 15:38–44
www.sciencedirect.com
Secondary cell wall patterning during xylem differentiation Yoshihisa Oda and Hiroo Fukuda Xylem cell differentiation involves temporal and spatial regulation of secondary cell wall deposition. The cortical microtubules are known to regulate the spatial pattern of the secondary cell wall by orientating cellulose deposition. However, it is largely unknown how the microtubule arrangement is regulated during secondary wall formation. Recent findings of novel plant microtubule-associated proteins in developing xylem vessels shed new light on the regulation mechanism of the microtubule arrangement leading to secondary wall patterning. In addition, in vitro culture systems allow the dynamics of microtubules and microtubuleassociated proteins during secondary cell wall formation to be followed. Therefore, this review focuses on novel aspects of microtubule dynamics leading to secondary cell wall patterning with a focus on microtubule-associated proteins. Address Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan Corresponding authors: Oda, Yoshihisa ([email protected]) and Fukuda, Hiroo ([email protected])
Current Opinion in Plant Biology 2012, 15:38–44 This review comes from a themed issue on Growth and Development Edited by Xuemei Chen and Thomas Laux Available online 9th November 2011 1369-5266/$ – see front matter Published by Elsevier Ltd. DOI 10.1016/j.pbi.2011.10.005
SND1/NST3 and NST1 were also identified as master regulators for xylem fiber differentiation [5–7]. These transcription factors form a subgroup in the NAC family [8,9]. Ectopic expressions of these genes induce ectopic deposition of secondary walls in accordance with their cell fates, for example, spiral and annular secondary walls by VND7, pitted secondary walls by VND6, and flat secondary walls by SND1 [10,11,12,13]. Further analyses demonstrate that NAC-type master transcription factors regulate the secondary wall synthesis as their downstream events [11,13]. Therefore, xylem cell differentiation involves molecular mechanisms underlying dynamic formation of cell wall structures. Additionally the use of these master genes in in vitro culture resulted in establishment of novel xylem cell differentiation systems [10,11]. It is well known that the secondary wall pattern is determined by cortical microtubules (MTs) that direct the movement of cellulose synthase complexes on the plasma membrane [14]. However, the machinery by which cortical MTs are arranged to form specific secondary wall patterns is largely unknown. Recently, some important plant MT-associated proteins (MAPs) were identified in relation to the secondary wall patterning. For example, AtMAP70 family proteins are involved in the formation of the secondary wall boundary [15]. MIDD1/RIP3 promotes MT depolymerization in future secondary wall pit areas, resulting in a secondary wall depletion domain [10]. These findings shed new insight into the MT organization mechanism regulating secondary wall patterning. Therefore, in this review we summarize recent progress of studies on secondary wall patterning with a focus on MAPs.
Introduction
MT organization in xylem vessel cells
Tracheary elements are characterized by their elaborate morphology and are the major conductive component of xylem, which functions in the transport of water and nutrients from the root to the whole plant body. Tracheary elements are dead cells surrounded by rigid patterned cellulosic secondary cell walls beneath the primary walls [1]. In tracheary elements, secondary walls are deposited in various patterns, such as annular and spiral in protoxylem, and reticulate and pitted patterns in metaxylem (Figure 1) [2]. Thus, secondary wall pattern is an important character of different xylem cells.
Most cortical MTs run beneath the secondary wall thickening whereas few cortical MTs lie beneath the region between the secondary walls. Disruption of MTs by drug treatments disorganizes secondary wall patterns, suggesting that cortical MTs regulate secondary wall patterning [16,17]. In Arabidopsis root vessels, cortical MTs are necessary for targeting cellulose synthase complexes to the specific sites through vesicle transport along actin cables [18–20]. These cortical MTs probably function in targeting the vesicles that contain cellulose synthase complexes and in controlling the trajectory of cellulose synthase complexes as observed in hypocotyl epidermis [14,21,22].
Xylem cell fates are controlled by transcriptional master genes [3]. Two NAM/ATAF/CUC (NAC) transcription factors, VND6 and VND7, direct metaxylem and protoxylem vessel differentiation, respectively [4]. Current Opinion in Plant Biology 2012, 15:38–44
Studies using the in vitro culture of isolated Zinnia mesophyll cells [23] visualized dynamic changes of the www.sciencedirect.com
Secondary cell wall patterning during xylem differentiation Oda and Fukuda 39
Figure 1
secondary wall formation and to know their function. In this context, some important secondary wall-related MAPs have been discovered. We describe below such MAPs after categorizing them into four classes according to their function.
MAPs involved in cortical MT assembly Katanin is an MT-severing MAP that is involved in cortical MT organization in both non-xylem and xylem cells. The Arabidopsis genome encodes a katanin gene, AtKTN1, whose mutation causes global disorganization of the cortical MT array and cellulose microfibril arrays in secondary and primary cell walls resulting in cell deformation and short organs [27,28]. In Arabidopsis hypocotyl epidermis cells, AtKTN1 is required to release the nucleated MTs from gamma tubulin complexes that are recruited beside existing cortical MTs [29]. Although it is not clear whether katanin functions in xylem cells similarly to those in hypocotyl epidermis cells, MT nucleation and severing should be an important process to organize the cortical MTs into distinct patterns of secondary wall deposition.
Current Opinion in Plant Biology
A collection of secondary wall patterns of xylem vessels in Arabidopsis plants. From left: spiral, reticulate, scalariform, and two pitted patterns. Scale bar represents 10 mm.
cortical organization of MTs during secondary wall formation in developing tracheary elements and confirmed that secondary wall patterns reflect the preceding localization of cortical MTs [24]. Recently, two Arabidopsis xylogenic culture systems were established: a culture in which boron and/or plant hormones are used as inducers of tracheary element differentiation [4,15,25] and a VND6-harboring culture in which estrogen induces VND6 and then metaxylem vessel differentiation [10]. These cultures allowed to introduce various cytoskeleton-related genes and follow the dynamics of their gene products during secondary wall deposition. By using cultures expressing GFP-tubulin, it was revealed that cortical MTs are gradually bundled and then followed by secondary wall deposition [25,26]. In differentiating cultured metaxylem vessel cells, rescue events of cortical MTs are inhibited in the future pit area, which causes the local disassembly of MTs to form an MT-free area [10]. These findings suggest that MT organization is regulated, at least in some part, in a secondary wall-specific manner. Therefore, it is important to find MAPs involved in www.sciencedirect.com
ZeMAP65-1 and AtMAP65-8, members of the MAP65 protein family, are preferentially expressed in xylogenic Zinnia mesophyll cells and Arabidopsis suspension cells, respectively [4,30]. An antibody against the conserved peptide of MAP65 proteins detects bundled cortical MTs in differentiating xylem cells [30]. Ectopic expression of ZeMAP65-1 in Arabidopsis cultured cells induces massive bundling of cortical MTs [30]. Therefore, these MAP65 members must be responsible for the bundling of the cortical MTs in xylem vessels. Because carrot MAP65 and AtMAP65-1, other members of the MAP65 protein family that act in non-xylem cells, also induce MT bundles by cross-linking each other [31,32], in general, this family may function in the assembly of MTs.
MAPs involved in oriented cellulose deposition FRA1, which encodes a kinesin motor protein of the kinesin-4 family, is expressed strongly in xylem, meristems, and parenchyma [33,34]. The mutation in the FRA1 locus decreases the mechanical strength of interfascicular fibers due to disorganization of cellulose microfibril alignment in the secondary walls. However, fra1 mutants do not differ significantly from the wild type in secondary wall composition, secondary wall thickness, or cortical MT organization [33]. Overexpression of FRA1 in plants increases layers of secondary walls with a remarkable decrease in the thickness of each secondary wall layer in xylem cells [34]. Because the number of secondary wall layers is dependent on changes in the orientation of cellulose microfibrils, all of these data suggest that FRA1 may function in the oriented deposition of cellulose microfibrils probably by regulating the cellulose synthesis machinery or the transport of vesicles carrying the secondary wall materials [34]. Current Opinion in Plant Biology 2012, 15:38–44
40 Growth and Development
Another MAP involved in secondary wall deposition is Populus MAP20 (PttMAP20), which is a plant-specific small protein containing a conserved TPX2 domain. PttMAP20 is co-upregulated in all types of populous xylem cells [35] with the secondary wall-associated cellulose synthase genes. PttMAP20 directly binds MTs in vitro and decorates MTs in vivo. Overexpression of PttMAP20 results in twisted shoot organs and shorter roots as frequently observed in plants in which other MAPs are overexpressed. Although the exact function of PttMAP20 is still to be demonstrated, a cellulose synthesis inhibitor 2,6dichlorobenzonitrile (DCB) was found to bind to PttMAP20 [35]. Recently, DCB treatment was shown to inhibit the mobility of cellulose synthase complexes at the plasma membrane [36]. Because DCB does not inhibit MT binding of PttMAP20, PttMAP20 may promote the activity of the cellulose synthesis along cortical MTs [35].
MAPs defining the boundary of secondary walls MAP70-5 and MAP70-1 belong to the plant-specific 70 kDa MAP family [37,38]. MAP70-5 was found to be specifically expressed during xylem differentiation in comprehensive expression analysis for over 200 MAPs using newly established xylogenic Arabidopsis cell culture [15]. Although MAP70-1 is constitutively expressed in the cell culture, these two proteins interact with each other and function in secondary wall patterning [15]. Overexpression of MAP70-5 and/or MAP70-1 increases the population of xylem cells with spiral secondary walls. By contrast, the knockdown for MAP70-5 or MAP70-1 by RNA interference increases the population of xylem cells
with pitted secondary walls. Knockdown for MAP70-5 or MAP70-1 causes dissociation of secondary wall thickenings from the plasma membrane in all types of the tracheary element. Indeed, MAP70-1 and MAP70-5 proteins appear to localize at the subpopulation of cortical MTs along the edge of secondary wall thickenings. On the basis of these results, the authors suggest that MAP70 proteins define the boundary of secondary wall deposition on the plasma membrane. Considering that MAP70-5 was indicated to stabilize MTs [38] and that similar patterns of secondary walls were observed in taxol-treated cells [25], one might assume that MAP70-5 protein affects secondary wall patterns by stabilizing cortical MTs. The mechanism of the distinct localization of these proteins remains to be determined.
MAPs preventing secondary wall deposition Using the VND6-inducible metaxylem vessel differentiation culture, MIDD1 was identified as a MAP that regulates secondary wall patterns [10]. MIDD1 is upregulated rapidly by VND6 and VND7, which induce metaxylem and protoxylem vessel differentiation, respectively [10,11]. MIDD1 directly binds MTs in vitro [10]. However, in differentiating metaxylem vessel cells, MIDD1 decorates only the subpopulation of cortical MTs in the secondary wall pits (Figure 2a). MIDD1 is a plant-specific small protein composed of only two coiled-coil domains. Domain analysis revealed that the first coiled-coil domain binds MTs and the second coiledcoil domain recognizes the plasma membrane domain beneath the secondary wall pits. Knockdown of MIDD1
Figure 2
(a)
MT
MIDD1
0 sec
72
48
24
96
(b)
Secondary wall
Pri r mary wall ri Pla asma s sm membr m ane
ROP MT MT
MT
MT
?
MIDD1 AtKinesin-13A
? Current Opinion in Plant Biology
Dynamics and function of MIDD1. (a) Time-lapse observation of cortical MTs (RFP-TUB6) and MIDD1 (MIDD1-GFP) in the differentiating xylem cell. Yellow arrowheads indicate growing MTs that are specifically labeled with MIDD1. Red arrowheads indicate shrinking MTs. Scale bar represents 2 mm. (b) Schematic illustration of a possible model for MIDD1 function. In this model, MIDD1 is anchored to the plasma membrane in secondary wall pits by GTP-bound ROPs, recruits AtKinesin-13A, and binds cortical MTs in the secondary wall pits to promote disassembly of cortical MTs. Current Opinion in Plant Biology 2012, 15:38–44
www.sciencedirect.com
Secondary cell wall patterning during xylem differentiation Oda and Fukuda 41
with RNAi causes failure of local MT disassembly, which results in producing pit-free flat secondary walls. Conversely, overexpression of MIDD1 decreases the density of cortical MTs. These results strongly suggest that MIDD1 is a crucial factor for MT disassembly in secondary wall pits [10]. It was reported that MIDD1 interacts with AtKinesin13A, a member of the Kinesin-13 family [39]. Animal Kinesin-13 proteins depolymerize MTs in an ATP-dependent manner [40,41]. AtKinesin-13A lacks the conserved neck region that is necessary for interaction between the motor domain and MTs to exert MT depolymerization activity [42]. Therefore, AtKinesin-13A is
unlikely to have MT depolymerization activity [41]. Indeed, this protein does not exhibit MT colocalization but localized to the Golgi apparatus [43]. However, it is plausible that MIDD1 combines AtKinesin-13A to cortical MTs and allows it to work for MT depolymerization. MIDD1 is accumulated at the MT plus end during MT shrinkage [10]. Similarly, Drosophila KLP59C, a member of Kinesin-13, accumulates at the MT plus end during MT shrinkage [44]. Therefore, a member (or members) of the plant Kinesin-13 family might depolymerize MTs together with MIDD1. Further studies are required to test this possibility.
Figure 3
Production of plasma membrane domains ROPs?
Local MT disassembly Without MIDD1
MIDD1 Kinesin-13A?
MIDD1
MAP70
Control of secondary wall boundary? MAP70 Cortical MT organization Katanin MAP65?
Oriented deposition of cellulose microfibrils MAP20 ? FRA1
Current Opinion in Plant Biology
A schematic illustration for a template organization model for secondary wall patterning. First, plasma membrane domains are produced by ROPs as a robust template for secondary wall patterns. Second, MIDD1 is recruited to the plasma membrane domains to promote local disassembly of cortical MTs. MAP70 may organize cortical MTs to define the boundary for secondary wall deposition to shift the secondary wall pattern. Katanin and MAP65 organize the cortical MTs through severing and bundling beneath the future secondary wall thickening. Finally, FRA1 and MAP20 control the oriented deposition of the cellulose microfibrils along the cortical MTs. www.sciencedirect.com
Current Opinion in Plant Biology 2012, 15:38–44
42 Growth and Development
The pit-specific MT association of MIDD1 depends on its second coiled-coil domain, which is anchored to the plasma membrane in secondary wall pits [10]. MIDD1 is a member of the ICR/RIP family of proteins, which are shown to interact with plant-specific Rac/Rho small GTPases (ROPs) [45,46]. Recently, it was demonstrated that MIDD1 is a ROP effector that binds to the GTP-bound form of ROPs [39]. It is well known that ROPs are localized at specific plasma membrane domains and are involved in cell polarity [47]. Regarding cortical MTs, ROP6 recruits its effector RIC1, which locally induces ordered cortical MTs to form indentations of leaf epidermal cells [48,49]. Therefore, it is plausible that ROPs anchor MIDD1 at the discrete plasma membrane domains. Indeed, deletion of the Cterminal part of the second coiled-coil domain comprising the ROP binding motif was enough to abolish their anchorage at the plasma membrane [10]. In summary, MIDD1 is likely to act as a scaffold protein that bridges a ROP, a Kinesin-13 and cortical MTs (Figure 2b).
Template organization model Recent studies of secondary wall patterning have focused on cortical MTs, MAPs, and cellulose synthesis. However, identification and characterization of MIDD1 raises another possibility, namely that distinct plasma membrane domains also participate in the secondary wall patterning. Such plasma membrane domains may localize specific molecules that affect MT organization and secondary wall deposition, which thereby act as a robust template for secondary wall patterns. As described above, ROPs are good candidate molecules for producing plasma membrane domains as a template. Indeed, small GTPases are involved in producing plasma membrane domains in yeast budding [50], cell migration [51], and neural development [52]. One possibility is that such templates of ROPs might be established stochastically by Turing’s reaction diffusion model [53]. Once such a template is organized, MIDD1 is recruited to the plasma membrane domains by the ROPs and then depolymerizes the cortical MTs on the template. Subsequently, MAP70 may organize cortical MTs to define the boundary for secondary wall deposition to shift the secondary wall pattern. Considering the difference between the RNAi phenotypes for MIDD1 and MAP70s, MIDD1 and MAP70s may not function antagonistically but rather, function in different stages: MIDD1 promotes local depletion of cortical MTs while MAP70s modify the shape of the MT-depleted domains. Then, katanin and MAP65 organize the cortical MTs through severing and bundling beneath the future secondary wall thickening. Finally, FRA1 and MAP20 control the orientation of the cellulose microfibrils upon the cortical MTs (Figure 3).
wall patterns. Further analysis of ROPs as a templateproducing candidate would be promising to prove the template model. Nevertheless, our knowledge is still fragmentary. Further identification and characterization of other secondary wall-related proteins, including MAPs, are required to unveil fully the regulatory mechanism for secondary wall patterns. Because different xylem cell types have distinct secondary wall patterns, comparison of cytoskeleton-related genes downstream of master transcription factors inducing different xylem cell types may be useful for the identification of such proteins. Indeed, overexpression of VND6, VND7, and SND1 induces the expression of genes for different sets of kinesins (AT2G47500, AT5G06670, and AT4G38950 by VND7; AT2G47500, AT5G06670, At5G27950, and At5g54670 by VND6; At5G27950 and At5g54670 by SND1) in addition to MIDD1 and MAP65-8 [11,13]. Computational simulation analysis is also powerful in integrating insights into secondary wall patterning. Importantly, these insights into secondary wall patterning should contribute to advancing our understanding of secondary wall development and how plant cells produce distinct plasma membrane domains and then a variety of cell wall structures.
Acknowledgements This work was supported partly by Grants-in-Aid from the Ministry of Education, Science, Sports and Culture of Japan (19060009) to H.F., from the Japan Society for the Promotion of Science to H.F. (23227001) and Y.O. (22870005), and from Bio-oriented Technology Research Advancement Institution, Japan (BRAIN) to H.F.
References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as: of special interest of outstanding interest 1.
Fukuda H: Tracheary element differentiation. Plant Cell 1997, 9:1147-1156.
2.
Turner S, Gallois P, Brown D: Tracheary element differentiation. Annu Rev Plant Biol 2007, 58:407-433.
3.
Ohashi-Ito K, Fukuda H: Transcriptional regulation of vascular cell fates. Curr Opin Plant Biol 2010, 13:670-676.
4.
Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T: Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 2005, 19:1855-1860.
5.
Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M: NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 2007, 19:270-280.
6.
Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M: The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 2005, 17:2993-3006.
7.
Zhong R, Demura T, Ye ZH: SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 2006, 18:3158-3170.
8.
Demura T, Fukuda H: Transcriptional regulation in wood formation. Trends Plant Sci 2007, 12:64-70.
9.
Zhong R, Ye ZH: Regulation of cell wall biosynthesis. Curr Opin Plant Biol 2007, 10:564-572.
Conclusions and perspectives In this review, we described recent advances in studies on the regulatory mechanism of secondary wall patterning, with a special focus on MAPs, and provided a template model of MT organization leading to distinct secondary Current Opinion in Plant Biology 2012, 15:38–44
www.sciencedirect.com
Secondary cell wall patterning during xylem differentiation Oda and Fukuda 43
10. Oda Y, Iida Y, Kondo Y, Fukuda H: Wood cell-wall structure requires local 2D-microtubule disassembly by a novel plasma membrane-anchored protein. Curr Biol 2010, 20:1197-1202. The authors established a high efficiency in vitro differentiation system for metaxylem vessels by making transgenic Arabidopsis cultured cells with inducible VND6. The authors identified MIDD1/RIP3 as a MAP and found that MIDD1/RIP3 is required in local cortical MT disassembly for secondary wall pit formation. This study implies the potential involvement of ROP GTPase signaling in secondary wall patterning. 11. Ohashi-Ito K, Oda Y, Fukuda H: Arabidopsis VASCULAR RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation. Plant Cell 2010, 22:3461-3473. The authors compared target genes of VND6 and SND1 and revealed that they commonly regulate secondary wall-related genes whereas only VND6 upregulated PCD-related genes. They also clearly showed that VND6 induces the secondary wall deposition in metaxylem pattern while SND1 induces uniform secondary walls of xylem fibers. 12. Yamaguchi M, Goue N, Igarashi H, Ohtani M, Nakano Y, Mortimer JC, Nishikubo N, Kubo M, Katayama Y, Kakegawa K et al.: VASCULAR-RELATED NAC-DOMAIN6 and VASCULARRELATED NAC-DOMAIN7 effectively induce transdifferentiation into xylem vessel elements under control of an induction system. Plant Physiol 2010, 153:906-914. 13. Yamaguchi M, Mitsuda N, Ohtani M, Ohme-Takagi M, Kato K, Demura T: VASCULAR-RELATED NAC-DOMAIN7 directly regulates the expression of a broad range of genes for xylem vessel formation. Plant J 2011, 66:579-590. This study revealed direct and indirect targets of VND7 involved in a wide range of processes of xylem vessel differentiation and demonstrated that VND7 can induce secondary wall deposition in the protoxylem pattern while NST3 induces flat secondary walls of fibers. 14. Paredez AR, Somerville CR, Ehrhardt DW: Visualization of cellulose synthase demonstrates functional association with microtubules. Science 2006, 312:1491-1495. 15. Pesquet E, Korolev AV, Calder G, Lloyd CW: The microtubule associated protein AtMAP70-5 regulates secondary wall patterning in Arabidopsis wood cells. Curr Biol 2010, 20:744-749. The authors newly established an in vitro xylogenic cell culture from Arabidopsis roots and performed expression analysis for over 200 MAPs. They found that AtMAP70-5 is upregulated in their culture system and they analyzed the function of MAP70. This study demonstrated that the expression level of MAPs contributes to the secondary wall patterns. 16. Hepler PK: Morphogenesis of tracheary elements and guard cells. Cell Biol Monogr 1981, 8:327-347. 17. Gunning BES, Hardham AR: Microtubules. Annu Rev Plant Biol 1982, 33:651-698. 18. Gardiner JC, Taylor NG, Turner SR: Control of cellulose synthase complex localization in developing xylem. Plant Cell 2003, 15:1740-1748. 19. Wightman R, Turner SR: The roles of the cytoskeleton during cellulose deposition at the secondary cell wall. Plant J 2008, 54:794-805. 20. Wightman R, Marshall R, Turner SR: A cellulose synthasecontaining compartment moves rapidly beneath sites of secondary wall synthesis. Plant Cell Physiol 2009, 50:584-594. 21. Crowell EF, Bischoff V, Desprez T, Rolland A, Stierhof YD, Schumacher K, Gonneau M, Hofte H, Vernhettes S: Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 2009, 21:1141-1154. 22. Gutierrez R, Lindeboom JJ, Paredez AR, Emons AM, Ehrhardt DW: Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat Cell Biol 2009, 11:797-806. 23. Fukuda H, Komamine A: Establishment of an experimental system for the study of tracheary element differentiation from single cells isolated from the mesophyll of Zinnia elegans. Plant Physiol 1980, 65:57-60.
www.sciencedirect.com
24. Fukuda H, Kobayashi H: Dynamic organization of the cytoskeleton during tracheary-element differentiation. Dev Growth Differ 1989, 31:9-16. 25. Oda Y, Mimura T, Hasezawa S: Regulation of secondary cell wall development by cortical microtubules during tracheary element differentiation in Arabidopsis cell suspensions. Plant Physiol 2005, 137:1027-1036. 26. Oda Y, Hasezawa S: Cytoskeletal organization during xylem cell differentiation. J Plant Res 2006, 119:167-177. 27. Burk DH, Liu B, Zhong R, Morrison WH, Ye ZH: A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 2001, 13:807-827. 28. Burk DH, Ye ZH: Alteration of oriented deposition of cellulose microfibrils by mutation of a katanin-like microtubulesevering protein. Plant Cell 2002, 14:2145-2160. 29. Nakamura M, Ehrhardt DW, Hashimoto T: Microtubule and katanin-dependent dynamics of microtubule nucleation complexes in the acentrosomal Arabidopsis cortical array. Nat Cell Biol 2010, 12:1064-1070. This study revealed that katanin functions in severing the branched cortical MTs to release them from their mother MTs. 30. Mao G, Buschmann H, Doonan JH, Lloyd CW: The role of MAP651 in microtubule bundling during Zinnia tracheary element formation. J Cell Sci 2006, 119:753-758. 31. Chan J, Jensen CG, Jensen LC, Bush M, Lloyd CW: The 65-kDa carrot microtubule-associated protein forms regularly arranged filamentous cross-bridges between microtubules. Proc Natl Acad Sci USA 1999, 96:14931-14936. 32. Smertenko AP, Chang HY, Wagner V, Kaloriti D, Fenyk S, Sonobe S, Lloyd C, Hauser MT, Hussey PJ: The Arabidopsis microtubule-associated protein AtMAP65-1: molecular analysis of its microtubule bundling activity. Plant Cell 2004, 16:2035-2047. 33. Zhong R, Burk DH, Morrison WH 3rd, Ye ZH: A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 2002, 14:31013117. 34. Zhou J, Qiu J, Ye ZH: Alteration in secondary wall deposition by overexpression of the fragile fiber1 kinesin-like protein in Arabidopsis. J Integr Plant Biol 2007, 49:1235-1243. 35. Rajangam AS, Kumar M, Aspeborg H, Guerriero G, Arvestad L, Pansri P, Brown CJ, Hober S, Blomqvist K, Divne C et al.: MAP20, a microtubule-associated protein in the secondary cell walls of hybrid aspen, is a target of the cellulose synthesis inhibitor 2,6-dichlorobenzonitrile. Plant Physiol 2008, 148:1283-1294. 36. DeBolt S, Gutierrez R, Ehrhardt DW, Somerville C: Nonmotile cellulose synthase subunits repeatedly accumulate within localized regions at the plasma membrane in Arabidopsis hypocotyl cells following 2,6-dichlorobenzonitrile treatment. Plant Physiol 2007, 145:334-338. 37. Korolev AV, Chan J, Naldrett MJ, Doonan JH, Lloyd CW: Identification of a novel family of 70 kDa microtubuleassociated proteins in Arabidopsis cells. Plant J 2005, 42:547555. 38. Korolev AV, Buschmann H, Doonan JH, Lloyd CW: AtMAP70-5, a divergent member of the MAP70 family of microtubuleassociated proteins, is required for anisotropic cell growth in Arabidopsis. J Cell Sci 2007, 120:2241-2247. 39. Mucha E, Hoefle C, Hu¨ckelhoven R, Berken A: RIP3 and AtKinesin-13A: a novel interaction linking Rho proteins of plants to microtubules. Eur J Cell Biol 2010, 89:906-916. This paper demonstrated that MIDD1/RIP3 is the effector of ROP GTPases and interacts with AtKinesin-13A. 40. Desai A, Verma S, Mitchison TJ, Walczak CE: Kin I kinesins are microtubule-destabilizing enzymes. Cell 1999, 96:69-78. 41. Moores CA, Milligan RA: Lucky 13-microtubule depolymerisation by kinesin-13 motors. J Cell Sci 2006, 119:3905-3913.
Current Opinion in Plant Biology 2012, 15:38–44
44 Growth and Development
42. Ovechkina Y, Wagenbach M, Wordeman L: K-loop insertion restores microtubule depolymerizing activity of a ‘‘neckless’’ MCAK mutant. J Cell Biol 2002, 159:557-562. 43. Lu L, Lee YR, Pan R, Maloof JN, Liu B: An internal motor kinesin is associated with the Golgi apparatus and plays a role in trichome morphogenesis in Arabidopsis. Mol Biol Cell 2005, 16:811-823. 44. Mennella V, Rogers GC, Rogers SL, Buster DW, Vale RD, Sharp DJ: Functionally distinct kinesin-13 family members cooperate to regulate microtubule dynamics during interphase. Nat Cell Biol 2005, 7:235-245. 45. Lavy M, Bloch D, Hazak O, Gutman I, Poraty L, Sorek N, Sternberg H, Yalovsky S: A novel ROP/RAC effector links cell polarity, root-meristem maintenance, and vesicle trafficking. Curr Biol 2007, 17:947-952.
48. Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z: Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 2005, 120:687-700. 49. Fu Y, Xu T, Zhu L, Wen M, Yang Z: A ROP GTPase signaling pathway controls cortical microtubule ordering and cell expansion in Arabidopsis. Curr Biol 2009, 19:1827-1832. The paper demonstrated that local ROP signaling regulates cortical MTs at subcellular level to induce polarized cell growth. 50. Kozubowski L, Saito K, Johnson JM, Howell AS, Zyla TR, Lew DJ: Symmetry-breaking polarization driven by a Cdc42p GEF-PAK complex. Curr Biol 2008, 18:1719-1726. 51. Fivaz M, Bandara S, Inoue T, Meyer T: Robust neuronal symmetry breaking by Ras-triggered local positive feedback. Curr Biol 2008, 18:44-50.
46. Li S, Gu Y, Yan A, Lord E, Yang ZB: RIP1 (ROP Interactive Partner 1)/ICR1 marks pollen germination sites and may act in the ROP1 pathway in the control of polarized pollen growth. Mol Plant 2008, 1:1021-1035.
52. Wong K, Pertz O, Hahn K, Bourne H: Neutrophil polarization: spatiotemporal dynamics of RhoA activity support a selforganizing mechanism. Proc Natl Acad Sci USA 2006, 103:3639-3644.
47. Yang Z: Cell polarity signaling in Arabidopsis. Annu Rev Cell Dev Biol 2008, 24:551-575.
53. Turing A: The chemical basis of morphogenesis. Philos Trans R Soc Lond B Biol Sci 1952, 237:37-72.
Current Opinion in Plant Biology 2012, 15:38–44
www.sciencedirect.com